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DOI: 10.1007/s11099-012-0054-2 PHOTOSYNTHETICA 50 (3): 411-421, 2012
411
Investigation of the ameliorating effects of eggplant, datura, orange
nightshade, local Iranian tobacco, and field tomato as rootstocks
on alkali stress in tomato plants
Y. MOHSENIAN, H.R. ROOSTA+, H.R. KARIMI, and M. ESMAEILIZADE
Department of Horticulture, Faculty of Agriculture, Vali-e-Asr University of Rafsanjan, 7718897111, Rafsanjan, Iran
Abstract
Among the most important quality parameters of irrigation water used for greenhouse crops, alkalinity of water is
considered critical due to its impact on soil or growing medium solution pH. In this study, plant growth, Fe content,
photosynthetic pigment content, maximal quantum yield of PSII photochemistry (Fv/Fm), performance index (PI), leaf
relative water content (LRWC), and soluble sugars concentration were investigated in nongrafted and grafted tomato
(Lycopersicon esculentum Mill. cv. Red stone) plants onto five rootstocks of eggplant (Solanum melongena cv. Long
purple), datura (Datura patula), orange nightshade (Solanum luteum Mill.), local Iranian tobacco (Nicotiana tabacum),
and field tomato (Lycopersicon esculentum Mill. cv. Cal.jn3), exposed to 0, 5, and 10 mM NaHCO3 concentrations, to
determine whether grafting could improve alkalinity tolerance of tomato. Significant depression of leaf area, leaf and
stem dry mass, shoot and root Fe content and LRWC under high NaHCO3 level was observed in both grafted and
ungrafted plants. The highest reduction in the shoot Fe content was observed at 10 mM sodium bicarbonate in control
plants (greenhouse tomato). Moreover, at high HCO3– level, the highest percentage of LRWC reduction was also
recorded in ungrafted plants. Values of Fv/Fm and PI decreased significantly at 5 and 10 mM NaHCO3 irrespective of
rootstock type. The present study revealed that soluble sugars content, photosynthetic pigments content, Fv/Fm and PI
values in plants grafted onto datura rootstock were higher than those in nongrafted and rest of the grafted plants. Thus,
the use of datura rootstock could provide a useful tool to improve alkalinity tolerance of tomato plants under NaHCO3
stress.
Additional key words: chlorophyll fluorescence; grafting; Lycopersicon esculentum; NaHCO3; performance index.
Introduction
The increase in urban population is imposing restrictions
on the use of water of good quality for irrigation of
cultivated plants (Carter et al. 2005). Water quality can
determine the crops that can or cannot be grown, the
methods for irrigation, and the requirement of water treat-
ments. Among the most important quality parameters,
alkalinity of water is considered critical due to its impact
on soil or growing medium solution pH (Petersen 1996).
Bicarbonate is the main ion that causes alkalinity and
imparts buffer capacity to water, and at concentrations
higher than 2 mM it can cause a significant suppression
in plant growth of sensitive species due to the increase in
water pH (Valdez-Aguilar and Reed 2010). The most
conspicuous symptom of excessive alkalinity is the
induction of interveinal chlorosis in the youngest leaves
and stunted growth (Valdez-Aguilar and Reed 2007).
Alkalinity-induced leaf chlorosis has been attributed to an
iron (Fe) deficiency due to decreased Fe uptake (Bertoni
et al. 1992) and/or Fe availability (Roosta 2011). Fe defi-
ciency reflects upon the physiology and biochemistry of
the whole plant, as Fe is an important cofactor of many
enzymes, including those involved in the biosynthetic
pathway of chlorophylls (Marschner 1995). Fe deficiency
decreases the leaf photosynthetic rate (Terry 1980) by
reducing the number of photosynthetic units per area
(Spiller and Terry 1980) and by lowering the actual
photosystem II (PSII) efficiency of the remaining units
(Morales et al. 1998). On the other hand, PSII is well
known for its sensitivity to abiotic stresses and hence it is
a good choice to study response and adaptation to stress
———
Received 10 December 2011, accepted 7 May 2012.
+Corresponding author; phone: +983913202053, fax: +983913202042, e-mail: roosta_h@yahoo.com
Abbreviations: Car – carotenoids; Chl – chlorophyll; DM – dry mass; Fv/Fm – maximal quantum yield of PSII photochemistry;
FM – fresh mass; LRWC – leaf relative water content; PI – performance index; PS – photosystem.
Acknowledgements: Here we would like to thank Vali-e-Asr University of Rafsanjan for financial support of the research. The results
presented in this paper are a part of M.Sc studies of the first author.
Y. MOHSENIAN et al.
412
by plants (Strasser et al. 2000). Environmental stresses
that affect PSII efficiency lead to a characteristic decrease
in Fv/Fm (Krause and Weis 1991). The Fv/Fm is a mea-
surement of the light energy transfer in dark-adapted
samples or the photochemical quantum yield of open PSII
centers (De Ell and Toivonen 2003).
Alkali stress has complex effects on root physiology
(Wang et al. 2012). High alkalinity can cause the loss of
the normal physiological functions of the roots,
destruction of the root cell structure, inhibit the
absorption of ions such as Cl–, NO3–, and H2PO4–, thus
greatly affecting the metabolism of K+ and Na+ and
disrupt metabolism homeostasis (Chen et al. 2011).
Organic acid secretion from the root has a crucial role in
alkali tolerance of plants (Yang et al. 2010). One way to
avoid or reduce losses in production caused by alkalinity
in high yielding genotypes would be to graft them onto
rootstocks capable of reducing the detrimental effect of
external pH on the shoot (Colla et al. 2010a).
Nowadays, grafting is used to reduce infections by
soil-born pathogens and to enhance the tolerance against
abiotic stresses (Schwarz et al. 2010). Among those are
saline soils (Colla et al. 2010b), soil-pH (alkalinity)
stress, nutrient deficiency, and toxicity of heavy metals
(Savvas et al. 2010). In relation to alkalinity tolerance,
Colla et al. (2010a) suggested that grafting provided an
alternative way to improve watermelon alkalinity tole-
rance. Nevertheless, no published data is available con-
cerning the effects of high alkalinity in the rooting
medium on agronomical, physiological and biochemical
responses of grafted tomato.
The purpose of this investigation is to study the effect
of different rootstocks on the greenhouse-tomato tole-
rance to alkalinity in hydroponic system, interpreted by
evaluating some vegetative parameters, photosynthetic
pigments content, Fv/Fm, PI, LRWC, soluble sugars, and
Fe content in grafted tomato plants.
Materials and methods
Plants, treatments, and growth conditions: A green-
house experiment was conducted in 2010 at the Agri-
college of Vali-e-Asr University of Rafsanjan (30°23′
06˝N, 55°55′30˝E), at 1,523 m a.s.l. To ensure similar
stem diameters at the grafting time, one week before the
planting of the greenhouse-tomato hybrid Lycopersicon
esculentum Mill. cv. Red stone as a scion plant, seeds of
five rootstocks of tomato were sown 5 mm deep in a
circular arrangement in each bucket containing perlite
medium (particles diameter of 1–2 mm). The five root-
stocks used in this study were eggplant (Solanum melon-
gena. cv. Long purple), datura (Datura patula), orange
nightshade (Solanum luteum Mill.), local Iranian tobacco
(Nicotiana tabacum), and field tomato (Lycopersicon
esculentum Mill. cv. Cal.jn3) which is commonly planted
in dry and saline areas of south Iran. Grafting was
performed when seedlings have developed 3–4 true
leaves using the touch splice and hole insertion grafting
methods, while ungrafted greenhouse tomato was used as
a control. Then the seedlings were transplanted into 4-L
plastic containers, containing aerated nutrient solution.
The basic nutrient solution used in experiment was
modified Hoagland and Arnon formulation (Hoagland
and Arnon 1950). This nutrient solution consisted of:
1 mM Ca(NO3)2, 1.5 mM KNO3, 0.25 mM KH2PO4,
0.5 mM MgSO4, 0.1 mM NaCl, 20 μM Fe-EDDHA,
7 μM MnSO4, 0.7 μM ZnCl2, 0.8 μM CuSO4, 2 μM
H3BO3, and 0.8 μM Na2MoO4. The experiment was
arranged as a factorial in the framework of a completely
randomized design with two factors, six grafting
combination (i.e., grafted or ungrafted plants) and bicar-
bonate (0, 5, and 10 mM NaHCO3) with 3 replications
consisting of 12 plants per treatment. Solutions were
changed completely every week in the first 2 weeks and
subsequently every 4th day. Solutions were prepared 24 h
before use to allow pH stabilization. pH were recorded
before renewal. Average initial pH was 7, 7.75, and 8.10
for solutions containing 0, 5, and 10 mM NaHCO3,
respectively. The plants were grown in a greenhouse with
13-h light phase (26 ± 3ºC) and 11-h dark phase (22 ±
3ºC). Greenhouse temperature was controlled by using
cool air from central cooler. The relative humidity was
52.4–63.2%. The photosynthetically active radiation was
500 μmol m–2 s–1.
Plant growth measurement: At the end of the experi-
ment the shoot length, leaf area and the number of leaves
produced for each treatment were recorded. Leaf area
(LA) was measured with an electronic area meter (Delta-
T Devices Ltd., Cambridge, UK). Six weeks after trans-
planting, the plant organs (roots, leaves, and stem) were
harvested, weighed and oven-dried (48 h at 72ºC) for
determination of leaf, stem and root dry mass.
Fe analysis: Dried samples of roots and shoots were
weighed separately and ground to pass a 40-mesh sieve.
The ground plant samples were dry-ashed at 500ºC for
4 h; the ashes dissolved in 10 ml HCl (2N) and made the
volume to 100 ml with distilled water. Content of Fe was
determined by atomic absorption spectrometry (model
GBC, AVANTA, Australia).
LRWC and soluble sugars content measurement: The
fully expanded fourth leaf from the top was used for
measuring LRWC as described by Weatherley (1950) and
calculated according to the formula: LRWC = [(FM –
DM)/(FM at full turgor – DM)] × 100, where FM is fresh
mass and DM dry mass. The content of soluble sugars in
leaves was measured according to the method of Irigoyen
et al. (1992).
EFFECT OF ROOTSTOCKS ON BICARBONATE TOLERANCE
413
Chlorophyll (Chl) and carotenoids (Car) contents:
Chl a, Chl b, total Chl, and Car were extracted with 80%
aqueous acetone (v/v) and were quantified using
of Arnon (1949) method. After filtering, absorbance
of centrifuged extracts was measured at 480, 510, 645,
652, and 663 nm using a spectrophotometer (U-2000,
Hitachi Instruments, Tokyo, Japan).
Chl fluorescence parameters measurement: Fv/Fm and
PI parameters were recorded by using a portable pocket
Plant Efficiency Analyzer (PEA, Hansatech Instruments
Ltd., Norfolk, UK). The pocket PEA optical interface was
mounted directly on to the front of the pocket PEA
control unit. It consisted of a single high intensity focused
LED which was positioned vertically above the sample
and provided up to 3,500 µmol m–2 s
–1 intensity with
a peak wavelength of 627 nm at the sample surface.
Three leaves were selected from each pot and preadapted
to dark period for 20 min by fixing special tags on each
leaf blade before measurements were taken. During dark
adaptation, all the reaction centers were fully oxidized
and available for photochemistry and any fluorescence
yield was quenched. After 20 min of dark adaptation, the
sensor cup was fitted on the leaf for measurement. The
vitality state of the tomato plants was characterized with
the performance index PI (Strasser et al. 2000).
Statistical analysis of variance and correlation were per-
formed by using the SAS software (SAS Institute, Cary,
NC, USA), if ANOVA determined that the effects of the
treatments were significant (P<0.05 for F-test), then the
treatment means were separated by LSD test.
Results
Growth: The results obtained from this experiment
showed that the stem dry mass was significantly affected
by NaHCO3, rootstock, with no significant NaHCO3 ×
rootstock interaction; whereas shoot length, leaf number,
leaf area, and leaf and root dry mass were highly influen-
ced by NaHCO3, rootstock and their interaction (Table 1).
As shown in Fig. 1, stem dry mass decreased drama-
tically with increasing NaHCO3 concentration in solution.
The highest stem dry mass was observed in control plants
(Fig. 2A). Whereas, even low bicarbonate concentration
(5 mM) decreased leaf number, leaf area, leaf dry mass
and root dry mass in control plants, but had no effect on
Table 1. Interactive effects of NaHCO3 levels and different rootstocks on shoot length, leaf number, leaf area and leaf and root dry
mass (DM) of tomato plants. Values are means ± SE of three replicates (n = 12). Different letters indicate significant differences
according to LSD test (P<0.05). ** –P<0.01; * – P<0.05.
Rootstock
N
aHCO3
[mM]
Shoot length [cm] Leaf number
[plant–1]
Leaf area
[cm2 leaf–1]
Leaf DM
[g plant–1]
Root DM
[g plant–1]
control 071.13 ± 3.25a11.72 ± 0.98a92.93 ± 5.29a2.88 ± 0.20a1.14 ± 0.07a
568.37 ± 2.99a 8.91 ± 0.46
b
c
d
71.09 ± 3.95
b
2.04 ± 0.30
b
c0.71 ± 0.09c–
f
10 56.66 ± 0.36
b
7.23 ± 0.39e
f
g48.25 ± 2.27c2.01 ± 0.09
b
c0.67 ± 0.03
d
e
f
Field tomato 041.41 ± 0.41cd 9.16 ± 0.88bcd 63.82 ± 6.73b2.12 ± 0.30b0.78 ± 0.06b–e
535.88 ± 1.44
d
e
f
8.25 ± 0.25
d
e
f
51.00 ± 1.66c1.71 ± 0.09
b
–e 0.59 ± 0.11e
f
g
10 34.76 ± 0.73
d
e
f
8.16 ± 0.16
d
e
f
46.15 ± 1.13c
d
1.16 ± 0.14
f
g
h
0.38 ± 0.10g
hi
Datura 023.76 ± 2.63gh 9.83 ± 0.16b51.42 ± 0.94c1.83 ± 0.11bcd 0.61 ± 0.13ef
523.37 ± 3.45g
h
8.80 ± 0.15
b
c
d
47.16 ± 2.05c
d
1.67 ± 0.15
b
–e 0.57 ± 0.01
f
g
10 23.17 ± 2.31g
h
8.33 ± 0.20c
d
e39.41 ± 2.89
d
e1.40 ± 0.09
d
e
f
0.50 ± 0.02
f
g
h
Orange
nightshade
033.16 ± 1.74ef 9.66 ± 0.88bc 32.41 ± 1.97efg 1.65 ± 0.12cde 0.98 ± 0.05ab
529.66 ± 0.88
f
g 6.50 ± 0.5g
ih
27.86 ± 0.50
f
g
h
1.16 ± 0.03
f
g
h
0.89 ± 0.07
b
c
10 22.66 ± 3.28g
h
5.36 ± 0.31
i
25.16 ± 0.72g
h
0.97 ± 0.06
f
g
h
0.54 ± 0.01
f
g
h
Tobacco 044.94 ± 2.23c12.77 ± 0.22a66.85 ± 2.56b2.60 ± 0.08a0.83 ± 0.08bcd
538.88 ± 3.46c
d
e 8.38 ± 0.45c
d
e47.07 ± 3.35
d
e1.33 ± 0.18e
f
g0.58 ± 0.09e
f
g
10 21.20 ± 3.03
h
7.00 ± 0.57e–
h
23.37 ± 0.69
h
1.00 ± 0.20
f
g
h
0.34 ± 0.02
i
g
h
Eggplant 032.74 ± 2.08ef 6.90 ± 0.1fgh 33.94 ± 1.80ef 1.10 ± 0.15fgh 0.21 ± 0.04ij
523.07 ± 4.03g
h
6.00 ± 0.28g
ih
27.75 ± 3.07
f
g
h
0.88 ± 0.16g
h
0.21 ± 0.02
ij
10 20.75 ± 0/90
h
5.73 ± 0.37
ih
25.22 ± 0.36g
h
0.72 ± 0.03
h
0.15 ± 0.02
j
A
NOVA DF Mean square
Rootstock 52137.60
**
14.94
**
2281.58
**
2.004
**
0.484
**
N
aHCO32583.15
**
44.33
**
2239.25
**
3.179
**
0.478
**
Rootstock ×
N
aHCO3
10 61.70
**
3.41
**
228.37
**
0.200
*
0.038
*
Y. MOHSENIAN et al.
414
Fig. 1. Effects of NaHCO3 concentrations (0, 5, and 10 mM) in
the nutrient solution on stem dry mass of tomato plants. The
results are the means ± SE of three replicates (n = 12). Different
letters indicate significant differences according to LSD test
(P<0.05).
shoot length (Table 1). At high concentration (10 mM) of
bicarbonate in control plants shoot length also decreased
(5 mM) decreased leaf number, leaf area, leaf dry mass
and root dry mass in control plants, but had no effect on
shoot length (Table 1). At high concentration (10 mM) of
bicarbonate in control plants shoot length also decreased
significantly. In the plants grafted on datura rootstock,
measured vegetative traits were not significantly affected
by bicarbonate application (Table 1). Considering to
tolerance of rootstocks to bicarbonate, field tomato was in
the second order after datura rootstocks. 10 mM NaHCO3
treatment caused a significant decrease in shoot length,
leaf number, leaf area, leaf and root dry mass of
ungrafted and grafted onto tobacco rootstock plants
(Table 1). The root-to-shoot ratio was significantly affec-
ted by rootstock, but not by NaHCO3 and their inter-
action. The highest root-to-shoot ratio was measured in
the plants grafted onto orange nightshade rootstock.
However the lowest values of root-to-shoot ratio were
recorded on those grafted onto eggplant and the ungrafted
plants (Fig. 2B).
Fe content: The shoot Fe content was significantly in-
fluenced by NaHCO3, rootstock and NaHCO3 × rootstock
interaction, but its content in roots was significantly
affected by rootstock and NaHCO3 × rootstock inter-
action, without significant effects caused by NaHCO3
(Table 2). Under normal growth condition, the content of
shoot Fe of grafted plants onto field tomato rootstock was
significantly higher than those of nongrafted and grafted
onto other rootstocks. The Fe content in shoots of tomato
plants decreased significantly as NaHCO3 levels in-
creased. The highest reduction in the shoot Fe content
was observed in control plants (greenhouse tomato) less
than 10 mM NaHCO3. Also at the same stress level,
plants grafted onto datura rootstocks showed the lowest
Fig. 2. The effect of different rootstocks on stem dry mass (A)
and root- to-shoot ratio (B) of tomato plants, the results are the
means ± SE of three replicates (n = 12). Different letters
indicate significant differences according to LSD test (P<0.05).
reduction in the shoot Fe content compared to unstressed
plants.
Data presented in Table 2 revealed that under high
alkalinity level (10 mM NaHCO3), the content of Fe in
roots was significantly increased in plants grafted onto
datura rootstock compared to unstressed plants, whereas a
significant decrease in Fe content was recorded in the
control plants (greenhouse tomato).
LRWC and soluble sugars content: LRWC was
significantly (P<0.01) affected by NaHCO3, rootstock,
and NaHCO3 × rootstock interaction (Table 2). With the
exception of orange nightshade and field tomato in the
other rootstocks an obvious decrease of LRWC was
observed with 5 mM NaHCO3 compared with plants
grown under unstressed conditions (Table 2).
When plants were treated with 10 mM NaHCO3,
LRWC decreased significantly in all plants compared with
plants grown under unstressed conditions, as the highest
rate of decline (77.12%) can be observed in control plants
(greenhouse tomato). Finally, with high NaHCO3 in the
nutrient solution, in comparison to control, the plants
were grafted onto field tomato and datura rootstocks,
showed the lower reduction of LRWC than those grafted
onto other rootstocks and the ungrafted plants.
EFFECT OF ROOTSTOCKS ON BICARBONATE TOLERANCE
415
Table 2. Interactive effects of NaHCO3 levels and different rootstocks on Fe content (in shoots and roots), leaf relative water content
(LRWC), and chlorophyll a (Chl a) of tomato plants. DM – dry mass, FM – fresh mass. Values are means ± SE of three replicates.
Different letters indicate significant differences according to LSD test (P<0.05). ** – P<0.01, * – P<0.05; ns – not significant.
Rootstock
N
aHCO3
[mM]
Shoot Fe
[mg kg–1(DM)]
Root Fe
[mg kg–1(DM)]
LRWC [%] Chl a
[mg g–1(FM)]
Control 0 58.86 ± 5.88b481.0 ± 28.4abc 64.28 ± 2.19a1.372 ± 0.125a
5 22.53 ± 1.41
ik
375.8 ± 40.2
b
–g 23.60 ± 0.68
h
1.096 ± 0.044
d
e
f
10 16.84 ± 0.64
k
317.7 ± 60.5e
f
g14.70 ± 0.73
i
0.997 ± 0.001
f
Field tomato 0 76.23 ± 3.05a456.2 ± 65.6a–e 60.16 ± 0.81ab 1.219 ± 0.006b–e
5 45.23 ± 0.92e
f
499.2 ± 101.7a
b
56.47 ± 0.82
b
c1.215 ± 0.018
b
–e
10 38.11 ± 1.62g
h
472.4 ± 44.5a–
d
53.93 ± 0.78c1.214 ± 0.023
b
–e
Datura 0 54.63 ± 1.53bc 327.1 ± 31.7d–g 32.26 ± 0.88f1.287 ± 0.054ab
5 46.58 ± 1.88
d
e296.0 ± 31.6
f
g27.28 ± 2.06g
h
1.288 ± 0.056a
b
10 42.33 ± 1.45e
f
g542.1 ± 349.9a26.94 ± 0.89g
h
1.241 ± 0.036a
b
c
Orange nightshade 0 39.70 ± 0.05fgh 470.6 ± 36.9a–d 56.12 ± 0.86bc 1.208 ± 0.035b–e
5 26.76 ± 1.16
j
397.6 ± 31.7a–
f
52.93 ± 3.35c1.133 ± 0.049c–
f
10 16.93 ± 1.49
k
347.5 ± 31.8c–g 45.70 ± 1.13
d
1.116 ± 0.050c–
f
Tobacco 0 51.83 ± 2.71cd 414.3 ± 56.8a–f 41.72 ± 0.34d1.225 ± 0.021a–d
5 33.50 ± 1.90
hi
303.9 ± 37.8
f
g37.35 ± 2.29e1.054 ± 0.072
f
10 25.48 ± 3.67
j
275.2 ± 28.2
f
g32.06 ± 1.04
f
0.998 ± 0.027
f
Eggplant 0 36.76 ± 1.89gh 257.9 ± 63.9g41.95 ± 0.84d1.220 ± 0.001b–e
5 27.64 ± 1.29
ij
333.3 ± 26.7c–g 31.73± 1.06
f
1.083 ± 0.067e
f
10 25.40 ± 0.73
j
354.0 ± 23.4
b
–g 28.19 ± 2.10
f
g1.025 ± 0.013
f
A
NOVA DF Mean square
Rootstock 5 945.8
**
29,730.5
**
1,117.9
**
0.040
**
N
aHCO3 2 3,179.3
**
5,062.8ns 1,191.8
**
0.116
**
Rootstock × NaHCO310 154.9
**
21,224.7
*
253.8
**
0.015
*
Fig. 3. The effect of different rootstocks on soluble
sugars content of tomato plants, the results are the
means ± SE of three replicates (n = 12). Differen
t
letters indicate significant differences according to
LSD test (P<0.05).
Results showed that the soluble sugars content was
significantly influenced by rootstock with values recor-
ded for plants grafted onto datura rootstock (1,432.71
μg g–1) being higher than plants grafted onto other
rootstocks and ungrafted plants (1,151.46 μg g–1) (Fig. 3).
Chl and Car contents: The Chl (a, b, and total) contents
were significantly affected by NaHCO3, rootstock had no
significant impact on Chl b content, but had a significant
effect on Chl a, total Chl and Car contents. Additionally,
the Chl a content was also significantly affected by
NaHCO3 × rootstock interaction (Table 2). Results
showed that sodium bicarbonate had no significant effect
on Chl a content in plants grafted onto field tomato,
datura and orange nightshade rootstocks. NaHCO3
treatment of 5 mM decreased Chl a content in control and
Y. MOHSENIAN et al.
416
Fig. 4. The effect of different rootstocks on total chlorophyll
(Chl) (A) and carotenoids (Car) contents (B) of tomato plants,
the results are the means ± SE of three replicates (n = 12).
Different letters indicate significant differences according to
LSD test (P<0.05).
plants grafted onto tobacco rootstocks. Meanwhile, com-
pared to the plants grown under unstressed conditions,
10 mM NaHCO3 significantly decreased Chl a contents
in ungrafted plants and grafted onto tobacco and eggplant
rootstocks (Table 2). The highest total Chl and Car
contents were recorded in the plants grafted onto datura
rootstock (Fig. 4A,B). Regarding to the effect of sodium
bicarbonate on Chl b and total Chl content, increasing the
concentration of NaHCO3 from 0 to 10 mM in the
nutrient solution decreased the Chl b and total Chl
content in leaves significantly, however, differences
between two levels of NaHCO3 (5 and 10 mM) were not
significant (Fig. 5A,B).
Fv/Fm and PI were significantly (P<0.01) affected by
NaHCO3 and rootstock, but not by their interaction. The
Fig. 5. Effects of NaHCO3 concentrations (0, 5, and 10 mM) in
the nutrient solution on chlorophyll (Chl) b (A) and total Chl (B)
contents of tomato plants. The results are the mean ± SE of
three replicates (n = 12). Different letters indicate significant
differences according to LSD test (P<0.05).
highest Fv/Fm and PI values were observed in plants
grafted onto datura rootstock (Fig. 6A,B). The lowest
Fv/Fm values were observed in greenhouse tomato
(control) plants. As shown in Fig. 6B, the lowest PI value
was observed in plants grafted onto orange nightshade
rootstock. Values of Fv/Fm and PI decreased significantly
at 5 and 10 mM NaHCO3 irrespective of rootstock type
(Fig. 6C,D).
Correlation coefficients analysis: The correlations
between shoot Fe concentration and all the photosynthetic
pigments were significant with the exception of Car
contents (Table 3); additionally the correlations between
Fe shoot and the fluorescence indices were very signifi-
cant. Total Chl content showed significant correlation
with fluorescence indices and shoot Fe content. Higher
correlations were found between Fv/Fm and shoot
Fe content.
Discussion
Researches have indicated that plants respond to elevated
NaHCO3 concentrations in soil or in growing medium
solution with decreased shoot and root growth (Campbell
and Nishio 2000). This could be due to either HCO3− or
Na+ (Pearce et al. 1999). Tomato, petunia (Bailey and
Hammer 1986), tobacco transplants (Rideout et al. 1995),
EFFECT OF ROOTSTOCKS ON BICARBONATE TOLERANCE
417
watermelon (Colla et al. 2010a) and lettuce (Roosta
2011), exhibited stunted growth when growing in either
soil or nutrient solution containing a high concentration
of HCO3−. Many of the test data show high pH as a key
factor in limiting plant growth and development under
alkaline conditions (Yang et al. 2007, 2008a,b; 2009a). In
the present experiment, significant depression in plant
growth parameters in bicarbonate-treated tomato plants
was observed, and that effect varied as a function of
rootstock (Table 1). 10 mM NaHCO3 treatment compared
to nonstress conditions caused a significant decrease in
shoot length, leaf number, leaf area, leaf and root dry
mass of ungrafted and grafted tomato onto tobacco
rootstock (Table 1). These phenomena may result from
nutritional damage, ion imbalance, and metabolic dis-
orders caused by alkali stress (Yang et al. 2009a).
Moreover, a high pH may lead to the lack of protons, the
destruction or inhibition of transmembrane electroche-
mical-potential gradients in root cells, and the loss of
normal physiological root functions such as ion
absorption (Yang et al. 2008a).
It is generally regarded that underground stresses
usually lead to increasing root/shoot ratio of biomass
(Szaniawski 1987), allowing the plant to have a greater
root surface area for absorption of water and nutrients
(Xiong et al. 2002). With the exception of eggplant
rootstock, the tomato plants grafted onto datura, orange
nightshade, field tomato, and tobacco rootstocks had
Fig. 6. Effect of the different rootstocks (A,B) and NaHCO3 concentrations (C,D) on maximal quantum yield of PSII photochemistry
(Fv/Fm) and performance index (PI) of tomato plants. The results are the means ± SE of three replicates (n = 12). Different letters
indicate significant differences according to LSD test (P<0.05).
Table 3. Correlation coefficients analysis in tomato plants between leaf relative water content (LRWC), performance index (PI), leaf
pigments (Car – carotenoids, Chl – chlorophyll), soluble sugars, maximal quantum yield of PSII photochemistry (Fv/Fm) and Fe
content in shoot and root. *** – P<0.001, ** – P<0.01, * – P<0.05; ns – not significant.
RWC PI Car Total Chl Chl b Chl a Soluble sugars Fv/Fm Root Fe
Shoot Fe 0.506*** 0.568*** 0.154ns 0.559*** 0.365** 0.583*** 0.074ns 0.601*** 0.359**
Root Fe 0.385
**
0.074ns 0.184ns 0.165ns 0.070ns 0.337
*
0.337
*
0.074ns
Fv/Fm 0.411
**
0.528
***
0.258ns 0.435
**
0.302
*
0.477
***
0.182ns
Soluble sugars
–
0.149ns 0.206ns 0.595
***
0.200ns 0.209ns 0.256ns
Chl a 0.447
***
0.351
**
0.328
*
0.526
***
0.256ns
Chl b 0.249ns 0.306
*
0.358
**
0.460
***
Total Chl 0.325
*
0.567
***
0.429
**
Car
–
0.108ns 0.363
**
PI
–
0.007ns
Y. MOHSENIAN et al.
418
higher values of root to shoot ratio than those ungrafted
(Fig. 2). These findings concur with the results of the
experiment done by Huang et al. (2009a) in cucumber
plants. Therefore, the better growth performance of
grafted- in comparison to ungrafted tomato plants
exposed to alkalinity stress might be attributed, at least to
some extent, to differential root growth under alkalinity
stress.
The results demonstrated that the alkali tolerance of
tomato plants can be improved by grafting onto datura
rootstock, for this reason we have observed that the
alkalinity has no significant effect on shoot length and
leaf and root dry mass of these plants. Earlier findings
showed that grafting of watermelon onto pumpkins
rootstocks may enhance alkalinity tolerance (Colla et al.
2010a). Alkalinity tolerance of tomato plants grafted onto
datura rootstock was due to the better uptake and
translocation of Fe to the shoot. Alkalinity reduces the
solubility of Fe due to the high pH associated with the
consumption of H+ by HCO3− (Valdez-Aguilar 2004), so
that under these conditions the range of inorganic Fe
availability is around 0.1–10% of the normal requirement
for optimal plant growth (Römheld and Marschner 1986).
Fe deficiency depresses the synthesis of chlorophyll,
which results in the decrease of photosynthetic products
affecting plant growth (Álvarez-Fernández et al. 2005).
The content of Fe in shoots of ungrafted and grafted
tomato plants was significantly decreased by NaHCO3
treatment. The highest reduction in the shoot Fe content
was observed in control plants (greenhouse tomato) under
10 mM sodium bicarbonate. On the other hand, at the
same stress level, plants grafted onto datura rootstocks
showed the lowest reduction in the shoot Fe content
compared to unstressed plants (Table 2). The higher
uptake and accumulation of Fe in tomato plants grafted
onto datura rootstock was the main mechanism that redu-
ces the detrimental effect of alkalinity (Fe-deficiency) on
plant growth.
Regardless of rootstocks, roots of tomato plants accu-
mulated larger amounts of Fe than shoots (Table 3), sug-
gesting that the critical process leading to chlorosis in
alkaline soils is Fe translocation from the root into the
shoot, which can be impaired by the alkaline apoplastic
pH due to high bicarbonate concentration (Colla et al.
2010a).
LRWC was used as a measure to estimate the stress
response (Jain and Chattopadhyay 2010). During stress
conditions plants need to maintain internal water potential
below that of soil and maintain turgor and water uptake
for growth (Ahmad and Sharma 2008). Lowering of
osmotic potential by osmolyte accumulation in response
to stress improves the capacity of the cell to maintain its
turgor pressure at low water potential. This appears to be
essential for physiological processes such as photosyn-
thesis, enzyme activity and cell expansion (Claussen
2005). Reduction in LRWC indicates a loss of turgor that
resulted in limited water availability for cell extension
process (Katerji et al. 1997). High alkalinity (10 mM
NaHCO3) treatment induced significant decreases in
LRWC in the stressed plants compared with those in the
control plants (Table 2). Similar results were obtained by
Yang et al. (2011). Under alkali stress, organic acids
might play an important role in maintaining ion balance
of cotton (Chen et al. 2011). In the present experiment,
under 10 mM NaHCO3 treatment, grafted plants onto
field tomato and datura rootstocks had the lowest
reduction in RWC of leaves in comparison with plants
grown in normal conditions. Less reduction in LRWC at
the tolerating rootstocks could be due to sufficient
osmotic adjustment (e.g. organic acids) in plant under
stress conditions. Therefore, less LRWC reduction in
datura and field tomato leaves results in more tolerance of
these rootstocks to alkalinity stress (Balaguer et al. 2002).
Parida and Das (2005) reported that lower osmotic
potential allows leaves to withstand a greater evaporative
demand without loss of turgor. This requires an increase
in osmotically active solutes either through uptake of
inorganic ions or synthesis of metabolically compatible
solutes (Munns and Tester 2008). Soluble sugars are
considered to be a compatible solute and their major
functions are osmoprotection, osmotic adjustment, carbon
storage and radical scavenging (Qun et al. 2010, Huang et
al. 2009b). In the present study, plants grafted onto datura
rootstock had higher soluble sugars content in the leaves
compared with other plants (Fig. 3). In accordance with
the present result, other researchers also reported that
tomato plants grafted onto S. lycopersicum have higher
soluble sugar content than self-rooted plants under NaCl
stress (Chen et al. 2005). Benefits of accumulation of
soluble sugars mentioned above might be part of the
reason for the increased alkalinity tolerance of tomato
plants grafted onto datura rootstock.
Chl and Car are the main photosynthetic pigments of
higher plants. In green plants Fe and Chl concentrations
are often well correlated (Miller et al. 1982). Similarly, in
the present study the correlation between Fe concen-
tration in shoots and Chl content quite evident (Table 3).
The solubility of Fe is known to decrease with increase in
pH and bicarbonate content, which are inter-related
through pH-buffering by equilibrium between H2CO3,
HCO3−, and CO32− (Bloom 2000). Thus, under Fe defi-
ciency conditions, the reduction in leaf Fe concentration
is often accompanied by a marked reduction of Chl levels
(Dasgan et al. 2003), by a significant, although less
intense, decrease in the Chl fluorescence (Nedunchezhian
et al. 1997), and by a reduction in photosynthesis
(Marschner 1995). At alkalinity stress, the contents of
Chl and Car in the barley plants decreased sharply with
increased stress in comparison to salinity stress. These
results indicate that high pH might decrease contents of
photosynthetic pigments (Yang et al. 2009b). Alkalinity-
induced leaf chlorosis has been attributed to a Fe
deficiency due to decreased Fe uptake (Bertoni et al.
1992) and/or Fe availability (Roosta 2011). Therefore, the
EFFECT OF ROOTSTOCKS ON BICARBONATE TOLERANCE
419
bicarbonate ions interfere with the uptake and transport of
Fe by tomato plants (Table 2), Chl content of plants
decreased as shown in Table 2 and Fig. 4A,B was not
unexpected (Gogorcena et al. 2004).
In accordance with our result in the datura rootstock
(Table 2, Fig. 5A), Pestana et al. (2005) reported that the
‘Troyer’ citrange rootstock was more effective in
overcoming the effects of the presence of bicarbonate
since these plants accumulated a greater amount of Fe
and Chl in the shoots.
According to the present result with the effect
of different rootstocks on Car content of tomato plants
(Fig. 5B), an increase in Car due to grafting was observed
in two tomato cultivars grafted onto a tomato hybrid
rootstock, under both nonsaline and saline conditions
(Fernandez-Garcia et al. 2004). Although the effects of
rootstock on Chl and Car levels have not been amply
discussed in relevant resources, the increase in the level
of Chl and Car in tomato due to datura rootstock by
means of their effects on photosynthesis and conse-
quently on other characteristics of the scion is most
probably one important result obtained in this study
regarding grafted tomato plants.
In the present study values of Fv/Fm decreased
significantly at 5 and 10 mM NaHCO3 irrespective of
rootstock type (Fig. 6C), suggesting the occurrence of
photoinhibition, and this could be a consequence of
damage to PSII (Demmig-Adams and Adams 1992). The
highest Fv/Fm values were observed in plants grafted onto
datura and field tomato rootstocks, which was attributed
to higher Chl a content in these rootstocks (Redondo-
Gómez et al. 2007). Values of Fv/Fm below 0.80 were
recorded for the plants of all treatments. This suggests
that photosynthetic apparatus was not fully developed or
slightly injured, which could occur in plants cultivated
under greenhouse conditions (Klamkowski et al. 2009).
In this experiment, significant correlation was observed
between Fv/Fm values and Fe content in shoots of tomato
plants (Table 3). Moreover, plants grafted onto both
rootstocks (datura and field tomato) had more Fe content
than those grafted onto other rootstocks and ungrafted
plants (Table 2). PSI and PSII complexes are both Fe-
containing proteins, Fe in PSII is important for water
splitting (Hulsebosch et al. 1996). Bertamini et al. (2001)
proved that the significant decrease in photosynthetic
electron transport is mainly due to the loss of PSII
activity in Fe-deficient grapevine leaves, and the loss of
PSII activity is due to the loss of D1 protein and 33 kDa
protein of the water-splitting complex. Our results
strongly proved this conclusion. But this might not be the
only factor limiting the electron transport in PSII.
PI is a sensitive indicator of photosynthesis (Strasser
et al. 2000). On the other hand, PI is a more complex
parameter reflecting overall efficiency of light absorption
as well as both light- and dark redox reactions (Strauss et
al. 2006). Therefore, PI is a potential indicator of current
physiological status of a plant, reflecting both disturbance
and acclimation of photosynthetic apparatus by changing
environmental conditions (Clark et al. 2000). Moreover,
PI is found to be a very sensitive parameter in different
crops and in most of environmental stresses (Strasser et
al. 2000, Jiang et al. 2006), which is in accordance with
our results achieved on grafted and ungrafted tomato
plants under alkalinity stress. In this experiment, PI value
decreased significantly in response to increase of
NaHCO3 concentration in tomato plants (Fig. 6D). Deng
et al. (2010) concluded that the performance index (PI)
gradually decreased with increasing of salinity-alkalinity,
so that under severe salinity-alkalinity stress in compa-
rison to control PI significantly decreased. They also
stated that nonstomatal limitation, i.e. decreased photo-
synthetic activity in PSII plays an important role in
decreased photosynthetic rate at high salinity-alkalinity.
The nonstomatal factors mainly depend on the cumulative
effects of leaf water and osmotic potential, biochemical
constituents (Sultana et al. 1999), contents of photosyn-
thetic pigments (Yang et al. 2008a), ion toxicities in the
cytosol (James et al. 2006), etc. We can conclude that
reduction of photosynthetic pigments under NaHCO3
treatments might be the part of the reason for PI reduc-
tion, which was confirmed by the results of correlation
analysis. Significant correlations were observed between
PI and total Chl content (Table 3). Our results showed
that the tomato plants with datura as rootstock exhibited a
higher value for total Chl content and greater PI than
other plants (Figs. 4A, 6B). The derived PI illustrated the
enhanced vitality of tomato plants with grafting onto
datura rootstock.
In conclusion, this study showed that plants grafted
onto datura rootstock exposed to excessive external
NaHCO3 level were capable of maintaining better
vegetative growth, strong capacity to accumulate Fe in
the aerial part, and the lower reduction of LRWC in
comparison to those grafted onto other rootstocks and the
ungrafted plants. Moreover, the present study revealed
that soluble sugars content, photosynthetic pigments
content, Fv/Fm, and PI values in plants grafted onto datura
rootstock were higher than those in nongrafted and other
rootstocks grafted plants. Overall, the use of datura root-
stock could provide a useful tool to improve alkalinity
tolerance of tomato plants under NaHCO3 stress.
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